Toxic Fungi of Western North America

by Thomas J. Duffy, MD

The amatoxic group

General description and occurrence

Fungi containing amanitin as their major toxin include species of Amanita, Lepiota, Galerina, Conocybe and possibly Cystolepiota. Regionally, there are 18 names or descriptions applied to fungi that are known or suspected to contain amanitin. These are Amanita phalloides, Amanita ocreata, Amanita bisporigera G.F. Atk., Amanita virosa sensu Schalkwijk-Barendsen (Sandy Lake, Alberta; possibly a 4-spored collection of Amanita bisporigera), Amanita virosa sensu Guzmán (Mexico), species close to Amanita bisporigera but with a negative or weak KOH reaction (Chiricahua Mountains, Arizona and neo-volcanic regions of central Mexico), Amanita marmorata ssp. myrtacearum Miller, Hemmes & Wong (Hawaii), Amanita magnivelaris Peck (per Guzmán, Mexico) , Amanita arocheae Tulloss, Ovrebo & Halling (Mexico), Galerina marginata (Fr.) Kühner, Galerina venenata, Conocybe filaris and the six Lepiota names given below. Some of the species have not had amanitin assays or produced known poisonings. In addition, the taxonomic status of some of these names is unclear. Guzmán and his colleagues tend to recognize European names, which may not be appropriate for New World material.

Species identified as Amanita virosa may be completely or at least largely the 4-spored form of the earlier-fruiting Amanita bisporigera, which has only 2 spores. There is a shift from 2 to 4 spores on each basidia as the fruiting season progresses. Specimens identified as Amanita bisporigera tend to be smaller than specimens identified as Amanita virosa. These are the species most commonly identified as causing amatoxin poisoning in Mexico.

The Amanitas

Species of Amanita are medium to large, often stately in stature with rather long stipes. (18a) The gills are typically free (not attached to the stipe), although there is some variation. In their button stages, amanitas somewhat resemble puffballs due to their enclosure in a universal veil surrounding the embryonic cap and stipe. As the cap expands, this veil is broken and usually leaves remnants on the cap and on the lower stipe with or without a clear-cut volva (or “cup”) at the base of the mushroom. Some amanitas have volval remnants in the form of basal rings, collar(s) or as a granular fragmentable “cup”.

Rain frequently washes off the thin veil remnants on the caps of Amanita phalloides and Amanita ocreata. Their thin collapsing volvas are readily left behind in the ground. A secondary veil from the edge of the cap to the stipe may or may not leave a ring on its upper portion. The spore print is white.

The white amanitas more or less fit the following description. The cap, veil, gills, ring, stipe and a ±sac-like volva are white. The caps are conic to convex or flat. The ring is usually skirt-like, often torn and may be persistent with age. The mushrooms are statuesque having caps (3) 5-9.5 (16) cm. broad and stipes (7) 14-20 (24) cm tall. Amanita bisporigera Atkinson is generally smaller than the others with caps 5-10 cm across and rarely has a slight tan tinge to the cap.

An additional amatoxic species, which looks like a grey or grey-brown Amanita phalloides but without the olive tones, occurs in northern Mexico: Amanita arocheae Tulloss, Ovrebo and Halling. (13a) This greyish “hongo gris” is distributed from north central Mexico to Andean Columbia. This species, Amanita arocheae Tulloss, Ovrebo and Halling, is also associated with oak.It has been assayed (as presumed Amanita phalloides) and found to contain amanitins. Presumably this species and the next two have produced toxic events in man or animals, but the author has no data on actual poisonings. In any event, the offending mushrooms would almost certainly have been misidentified as Amanita phalloides.

Amanita marmorata ssp. myrtacearum Miller, Hemmes & Wong grows in Hawaii’s Eucalyptus and Acacia forests along with Casuarina (Iron Wood) and Melaleuca (Paper Bark). This presumably amatoxic species has a cap, which is pure white to greyish and marmorate (blotchy or veined like marble). The ring is membranous and may disappear at maturity. The gills are close together and remain white. The volva is white and saccate.

Amanita longitibiale Tulloss, Pérez-Silva & T. Herrera, another of these presumably amatoxic species, is found in the pine and fir of neo-volcanic central Mexico. This slender member of section Phalloideae (Fr.) Quélet has caps that are pale yellow, aging pale grey to umbrinous. (13a,b)

In California, both Amanita phalloides and Amanita ocreata cause deadly encounters not infrequently in wet years; in Europe a dry year with consequently rare amatoxin poisonings is usually a good year for local wines. No such association has been shown in California, but pinot noir would be the most likely grape to show such a correlation. There has been at least one death from Amanita ocreata poisoning in Oregon. (19)

The Lepiotas

The genus Lepiota also has white spores and free gills, but with no volva. A minority have an annulus or an obvious annular zone. The genus Lepiota in the narrow sense contains a preponderance of small and often, fragile, fungi; typically having caps less than 6 cm wide (usually 1-4 cm across). These smaller mushrooms contain the amatoxins. Their caps are dry and often have small blackish, brown or reddish brown scales forming concentrically as the cap disc expands. The scales do not wash off, being intrinsic parts of the cap. Some species bruise an immediate bright red; others do not bruise, or more slowly bruise some shade of brown to blackish. The white or yellow gills are close together and the stipe breaks cleanly from the cap. A ring may be present, but it often collapses to just a bare outline on the stipe and is rarely prominent. The stipe below the ring area is usually scaly. There is no volva. The spore print is white to cream. All of the species considered here have European names and many of our species are probably not the same. The toxic species are: Lepiota helvelola, Lepiota josserandii, Lepiota castanea, Lepiota subincarnata and possibly Lepiota clypeolaria.

The numerous Lepiota species are even more difficult than the Amanita species to sort out: whether they have produced poisoning or not, whether amanitin has been detected or not and whether U.S. counterparts are the same as the European species. Dr. Else Vellinga presented an account of the genus based on the European work of Gérault, Girre and Besl at the Mycological Society of San Francisco October 2001 and noted that most lepiotas have an unpleasant rubber-like smell, with a sweet component. However, most of the toxic ones (Lepiota josserandii, L. helveola, L. subincarnata) often have a seductively sweetish smell.

Two small species on the west coast are highly toxic—Lepiota josserandii Bon & Boiffard (=helveola sensu Josserand) and what has been assumed to be Lepiota helveola Bres. (=helveola sensu Huijsman). Although our Lepiota helveola looks remarkably like the print of this species in Fries’ Icones, some of the microscopic features suggest that the Icones’ fungus may actually be Lepiota subincarnata Lange, another European taxon. (25),(26) Both Lepiota helveola and Lepiota josserandii have caused severe, but not fatal poisonings in California. Lepiota josserandii has caused one death in Vancouver, British Columbia. (26a)Lepiota “helveola” also occurs in Mexico. (27)

The possibly toxic European Lepiota clypeolarioides Rea, or one very like it, is present along our west coast. This species, however, is so poorly delineated in Europe, that it is not clear as to exactly what mushroom the name refers. Dr. Joe Ammirati gives a description of U.S. material from California in Poisonous Mushrooms of the Northern United States and Canada. (125)

Lepiota castanea Quél. and Lepiota oregonensis are probably toxic. Two other species, Lepiota brunneoincarnata and Lepiota felina, may be toxic. Other species, which are closely related to known toxic European species such as Cystolepiota heteri, are suspect. It is also not clear that Cystolepiota heteri occurs in the United States. Lepiota elaiophylla, a greenhouse mushroom, may also be toxic; if so, the toxin is probably not an amatoxin.

Only Lepiota helveola and Lepiota josserandii have produced definite amatoxin poisoning. Both of these species have an annulus or annular zone, although the thin tissue may weather away in age.

Lepiota helveola has a more or less vinaceous medium brown cap except between the scales where the underlying tissue is whitish, 1.5-4 cm wide, dry, convex becoming flatter in age, with or without an umbo (small knob) at the center, with flat concentric scales almost all towards the margins of the cap. The gills are white to a yellowish buff and free from the stipe. The cap breaks readily free from the stipe, which is 2.5-4.5 cm long and 4-9 mm wide. There is a more or less membranous ring, which may collapse on the stipe; above it, the whitish stipe is smooth and below it, the stipe is thinly covered with scales, which are concolorous with the cap.

Lepiota helveola

Lepiota josserandii has a dry cap, 2-4.5 cm wide, convex becoming flatter in age, with or without an umbo, the cinnamon brown to dull reddish cuticle broken into concentric scales over the whitish underlying tissue. These flat scales develop as the cap enlarges; they are more conspicuous than in Lepiota helveola and begin closer to the center of the cap. The gills are white to pale yellow, close together and free or slightly attached to the stipe. Young specimens have a cobweb-like partial veil (from the cap margin to the stipe), which quickly collapses to a ragged line on the stipe with aging. Below the ring area, the stipe is scaly and concolorous with the cap. The stipe is 2.5-5 cm long and 5-10 mm wide.

Most of the edible members of the Lepiota family are in the genera Macrolepiota, Chlorophyllum and Leucoagaricus. None of these three genera is known to contain amatoxins, although Chlorophyllum molybdites may cause severe vomiting and diarrhea.

The Galerinas

Galerina autumnalis (Pk.) A. H. Smith & Sing. and Galerina marginata (Fr) Kühner are now considered conspecific species. The difference between the two species was thought to be the presence of a gelatinous cap layer in Galerina marginata, but this feature is minimal and inconstant. The proper species epithet is marginata, since that name has priority under the International Botanical Code of Nomenclature.

Galerina marginata is a small fungus with convex to flat, viscid to moist caps 1.5-6.5 cm across and honey-colored to brown, the disc usually the darkest, the cap fading to dull tan or buff. The flesh is thin, white to ochre brown. The gills are broadly attached to subdecurrent on the stipe, close together and usually concolorous with the cap. The stipe is 3-9 mm across and 3-8 cm long with an evanescent thin fibrillose-membranous ring. The stipe is paler than the cap above the ring, buff to pale brown and below is ± concolorous or more reddish brown, ± shaggy below and with an evanescent coating of pale fibrils at the base, often displaying a white mycelial tuft. This species fruits scattered to abundantly and may be clustered on ± decayed logs, buried wood, in deep moss or occasionally along woodland paths.

Galerina marginata as identified in California had a positive Meixner test for amatoxins in only 1 of 3 specimens tested at the MSSF Fungus Fairs; an additional 3 tested by the author had 2 positive tests (one weakly so). In Europe, some specimens of Galerina marginata have also lacked amatoxins. The Internet site www.uio.no/conferences notes that European and American taxa were compatible in culture studies done at Ron Peterson’s laboratory in Knoxville; additionally, nuclear rDNA studies done by Gulden, G. et al. showed that material identified earlier as Galerina autumnalis or Galerina marginata were compatible with a single species. (23a)

The fact that some species identified as Galerina marginata (or Galerina autumnalis) are negative for amatoxin is quite misleading as this species is often deadly in small amounts and has been postulated to contain other toxins. A small piece chewed to confirm its mealy flavor provoked a hospital stay for one experimenter. In one of the exceedingly rare cases of severe poisoning in the case of a “grazing child”, a small girl was killed by what appeared to be a similarly small piece. (27a)

Galerina venenata with a lighter reddish-brown cap fades to near white and is usually grouped in grassy areas (possibly on buried wood). This species has been reported from Oregon and Washington and would be expected in British Columbia. A few have been found on lawns in Idaho. Although the species differs from Galerina marginata in color and habitat, molecularly it does not and Gulden et al placed all of these species along with Galerina oregonensis under the subgenus Naucoriopsis, which then forms a distinct infrageneric unit.

Galerina venenata Smith has the rare historical novelty that the species (or at least variety) was discovered and named only after it caused a poisoning. Two Oregon artists in 1953 thought that they had found the edible Amanita fulva (Schaeff.) Fr., but they encountered the genus Galerina instead. The specimens could not be identified by the Oregon Mycological Society and were air mailed to Dr. A.H. Smith, who later named this new fungus Galerina venenata. (28) Galerinas are most common in the fall, but may fruit in the spring. The spores are minutely wrinkled or ornamented under the oil immersion lens of the microscope and have no germ pore; the spore print is rusty to tobacco brown.

Conocybe filaris

Conocybe filaris (Fr.) Kühner is a small brown fungus has a smooth to finely wrinkled cap. When moist, the gills may be seen through the thin flesh at the margins as fine striations; when dry the cap becomes ± opaque and dull tan. The moist cap is typically brown to tawny brown, sometimes an attractive orangish brown. The margins may be a lighter cinnamon, medium brown or yellowish brown. The cap is ±conical when young, but expands to convex or flat. The cap is typically 1-2.5 cm across when mature; the young conic caps may measure only 3-4 mm across and up to 4-5 mm measured vertically. The pallid gills are thin and close together, soon becoming brown with an orange to yellow tinge from the cinnamon brown spores. The gill edges are finely fimbriate when young.

The fragile stipe is hollow, usually longer than the cap (1.5-5 cm) and has a width no more than 3mm. The partial veil leaves a buff to white, skirt-like, loosely attached, fibrillous-membranous ring with its upper surface striate-grooved where it separated from the gills. It is somewhat felty and may be tinged with the color of the adjacent stipe. The ground color of the scurfy stipe above this ring is a light orange-yellow, yellow brown or light brown and below the ring the more fibrillose stipe is dark brown to dark rusty brown. The spore print is cinnamon to nutmeg brown.

This potentially deadly species is so small that it is unlikely to cause death in an adult. Dr. Harry Thiers of San Francisco State University reported a non-fatal poisoning in a child to the Mycological Society of San Francisco. The poisoning occurred not long after Dr. Thiers moved to San Francisco (probably in the early 1960’s). The child was “grazing” on the lawn at San Francisco State University, but no clinical details are available. (29) Not all specimens of Conocybe (Pholiotina) filaris contained amatoxins on the basis of Meixner testing performed by the Mycological Society of San Francisco (MSSF) and by the Los Angeles Mycological Society (LAMS). (30)

There appear to be no other reports of illness from this mushroom, which is found in grass, moss and on wood chips or soil near rotting wood or plant debris. There are a number of similar Conocybe species, which have not been studied for possible amatoxins.